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PMID: 19716801 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

Retinal dynamics during light activation of rhodopsin revealed by solid-state NMR spectroscopy.

Biochimica et biophysica acta ·Vol. 1798 ·No. 2 ·2010-02-00 ·Pages 177-93

Brown MF, Salgado GF, Struts AV

Abstract

Rhodopsin is a canonical member of class A of the G protein-coupled receptors (GPCRs) that are implicated in many of the drug interventions in humans and are of great pharmaceutical interest. The molecular mechanism of rhodopsin activation remains unknown as atomistic structural information for the active metarhodopsin II state is currently lacking. Solid-state (2)H NMR constitutes a powerful approach to study atomic-level dynamics of membrane proteins. In the present application, we describe how information is obtained about interactions of the retinal cofactor with rhodopsin that change with light activation of the photoreceptor. The retinal methyl groups play an important role in rhodopsin function by directing conformational changes upon transition into the active state. Site-specific (2)H labels have been introduced into the methyl groups of retinal and solid-state (2)H NMR methods applied to obtain order parameters and correlation times that quantify the mobility of the cofactor in the inactive dark state, as well as the cryotrapped metarhodopsin I and metarhodopsin II states. Analysis of the angular-dependent (2)H NMR line shapes for selectively deuterated methyl groups of rhodopsin in aligned membranes enables determination of the average ligand conformation within the binding pocket. The relaxation data suggest that the beta-ionone ring is not expelled from its hydrophobic pocket in the transition from the pre-activated metarhodopsin I to the active metarhodopsin II state. Rather, the major structural changes of the retinal cofactor occur already at the metarhodopsin I state in the activation process. The metarhodopsin I to metarhodopsin II transition involves mainly conformational changes of the protein within the membrane lipid bilayer rather than the ligand. The dynamics of the retinylidene methyl groups upon isomerization are explained by an activation mechanism involving cooperative rearrangements of extracellular loop E2 together with transmembrane helices H5 and H6. These activating movements are triggered by steric clashes of the isomerized all-trans retinal with the beta4 strand of the E2 loop and the side chains of Glu(122) and Trp(265) within the binding pocket. The solid-state (2)H NMR data are discussed with regard to the pathway of the energy flow in the receptor activation mechanism.

MeSH Terms
Animals Humans Light Lipid Bilayers/chemistry Magnetic Resonance Spectroscopy/methods Protein Structure, Secondary/physiology,radiation effects Retinaldehyde/chemistry,metabolism Rhodopsin/chemistry,metabolism
Chemicals
Lipid Bilayers Rhodopsin Retinaldehyde
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Brown Michael F
Department of Chemistry, University of Arizona, Tucson, AZ 85721, USA; Department of Physics, University of Arizona, Tucson, AZ 85721, USA. mfbrown@u.arizona.edu
Salgado Gilmar F J
Struts Andrey V
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Article Info
Journal
Biochimica et biophysica acta
Abbr.
Biochim Biophys Acta
ISSN
0006-3002
DOI
10.1016/j.bbamem.2009.08.013
Email
mfbrown@u.arizona.edu
Published
2010-02-00
Epub
2009-00-28
Pages
177-93
Language
English
Region
Netherlands
NLM ID
0217513
PMCID
PMC5233717
Subset
IM
Grants
NEI NIH HHS · R01 EY012049 · United States
NEI NIH HHS · R01 EY018891 · United States
NEI NIH HHS · EY018891 · United States
NEI NIH HHS · EY012049 · United States
External Links
PubMed source DOI: 10.1016/j.bbamem.2009.08.013 PMC Full Text
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